Temperature effects on genetic and physiological regulation of adaptive plasticity

Abstract

This thesis contributed to a broader understanding of the genetic and physiological mechanisms that regulate developmental plasticity represented by butterfly wing color patterns. We found that different groups of cells within the same tissue have sensitivities and patterns of response that are distinct for the external environmental cue and for the internal hormonal signal. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein, and that manipulating pupal ecdysteroid levels is sufficient to mimic in direction and magnitude the shifts in adult reproductive resource allocation. We explored the effect of alleles of large effect on wing pattern on plasticity by characterizing thermal reaction norms for the size of eyespot rings for Bicyclus anynana mutants. Genotypes with alleles affecting eyespot size and color were the most sensitive to variation in developmental temperature. To explore genotype, temperature, and genotypextemperature effects on B. anynana development, we derived artificial selection lines expressing wet or dry-season-like phenotypes and, we characterized thermal reaction norms for a wider range of temperatures. Our results provided evidence for significant GxE effects, and also revealed a possible new color appearing at the most extreme low temperatures.

Summary

Developmental plasticity is an important strategy for adaptation to fluctuating environments. Such plasticity has one of its most compelling examples in seasonal polyphenism in butterflies; individuals can have different wing patterns and life-histories in alternating seasons. Previous studies have shown that the mechanism that mediates seasonal polyphenism involve ecdysteroids hormones; with alternative seasonal forms being characterized by differences in the timing of hormone increase after pupation. This thesis will contribute to a broader understanding of the genetic, developmental and physiological mechanisms that regulate developmental plasticity represented by temperature-regulated variation in butterfly wing color patterns. We will focus on a lab model for the study of adaptive phenotypic plasticity: color patterns on the wings of Bicyclus anynana butterflies. The adaptive value of the altern ative se asonal phenotypes in this species is well documented, and their underlying physiological underpinnings have started to be explored, however how animals perceive and assess temperature and how that influences development is still a black box.

We studied the integration of response of different traits by combining the analysis of changes induced by temperature in hormone physiology and traits development that lead to changes in phenotype. For that purpose, we explored the effects of manipulating external temperature, and internal levels of the active form of ecdysone and analyze phenotypic effects on different wing pattern and life-history traits. We also explored the mechanism for local sensitivities to systemic levels of ecdysone by testing the hypothesis that groups of cells that responded differently to ecdysone manipulations would differ in expression of ecdysone receptor. Additionally, we tested the ecological consequences of any hormone-induced changes in morphology and physiology observed by manipulating ecdysteroid at a single temperature and injection time point, and monitoring the effects on multiple aspects of adult fitness. We found that different groups of cells within the same tissue have sensitivit ies and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein. We also show that manipulating pupal ecdysteroid levels is sufficient to mimic in direction and magnitude the shifts in adult reproductive resource allocation normally induced by seasonal temperature. Crucially, this allocation shift is accompanied by ch anges in ecologically relevant traits, including timing of reproduction, lifespan and starvation resistance. Together, our results support a functional role for ecdysteroids during development in mediating strategic reproductive investment decisions in response to predictive indicators of environmental quality.
Genotypes can differ in many properties of reaction norms such as height, slope, or shape. We explored the effect of alleles of large effect on wing pattern on plasticity therein. To achieve this goal, we characterized thermal reaction norms for the size of eyespot color rings for B. anynana mutants with altered eyespot size and/or color composition. In addition, we explored standing genetic variation for alternative plastic phenotypes. To explore genotype (G), temperature (T), and GxT effects on B. anynana development, we derived artificial selection lines expressing extreme wet season-like or dry-season-like phenotypes at intermediary temperatures and, we characterized thermal reaction norms for several traits for a wider range of temperatures than is usually explored in this species to characterize the shape of reaction norms. Our results show variation between genetic stocks in the height, slope and shape of reaction norms providing evidence for significant GxE effects. G enotypes with alleles affecting eyespot size and color were the most sensitive to variation in developmental temperature. Our preliminary results also show that, for both sexes, there is a significant GxT interaction which confirms mean differences between the unselected stock and artificial selected lines responses in shape and height of reaction norms across temperature. Additionally, we show for wing background color, that for low temperatures there are three groups of pigments and for high temperatures four well distinct groups. Our preliminary results also revealed a possible new color appearing at the most extreme low temperatures.